Fibroblast activation protein drives tumor metastasis via a protease-independent role in invadopodia stabilization.

Humans Female Podosomes / metabolism Cell Line, Tumor Peptide Hydrolases / metabolism Neoplasm Invasiveness / pathology Breast Neoplasms / pathology Membrane Proteins / metabolism Serine Endopeptidases / metabolism Fibroblasts / metabolism Extracellular Matrix / metabolism Melanoma, Cutaneous Malignant
CP: Cancer MT1- MMP TWIST1 breast cancer extracellular matrix fibroblast activation protein invadopodia invasion matrix degradation tumor metastasis

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
31 10 2023
Historique:
received: 07 03 2023
revised: 09 08 2023
accepted: 03 10 2023
medline: 6 11 2023
pubmed: 20 10 2023
entrez: 20 10 2023
Statut: ppublish

Résumé

During metastasis, tumor cells invade through the basement membrane and intravasate into blood vessels and then extravasate into distant organs to establish metastases. Here, we report a critical role of a transmembrane serine protease fibroblast activation protein (FAP) in tumor metastasis. Expression of FAP and TWIST1, a metastasis driver, is significantly correlated in several types of human carcinomas, and FAP is required for TWIST1-induced breast cancer metastasis to the lung. Mechanistically, FAP is localized at invadopodia and required for invadopodia-mediated extracellular matrix degradation independent of its proteolytic activity. Live cell imaging shows that association of invadopodia precursors with FAP at the cell membrane promotes the stabilization and growth of invadopodia precursors into mature invadopodia. Together, our study identified FAP as a functional target of TWIST1 in driving tumor metastasis via promoting invadopodia-mediated matrix degradation and uncovered a proteolytic activity-independent role of FAP in stabilizing invadopodia precursors for maturation.

Identifiants

DOI: 10.1016/j.celrep.2023.113302 PMID: 37862167
pubmed: 37862167
pii: S2211-1247(23)01314-1
doi: 10.1016/j.celrep.2023.113302
pii:
doi:

Substances chimiques

Peptide Hydrolases EC 3.4.-
Membrane Proteins 0
Serine Endopeptidases EC 3.4.21.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

113302

Subventions

Organisme : NCI NIH HHS
ID : R01 CA262794
Pays : United States
Organisme : NCI NIH HHS
ID : F31 CA200271
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007752
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA206880
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA174869
Pays : United States
Organisme : NCI NIH HHS
ID : T32 CA009523
Pays : United States
Organisme : NCI NIH HHS
ID : F32 CA206227
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA236386
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA023100
Pays : United States

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no conflict of interest.

Auteurs

Maurish Bukhari (M)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Navneeta Patel (N)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Rosa Fontana (R)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Miguel Santiago-Medina (M)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Yike Jiang (Y)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Dongmei Li (D)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Kersi Pestonjamasp (K)

Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA.

Victoria J Christiansen (VJ)

William K. Warren Medical Research Center, Department of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA.

Kenneth W Jackson (KW)

William K. Warren Medical Research Center, Department of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA.

Patrick A McKee (PA)

William K. Warren Medical Research Center, Department of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA.

Jing Yang (J)

Department of Pharmacology, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA; Department of Pediatrics, University of California, San Diego, School of Medicine, La Jolla, CA 92093, USA. Electronic address: jingyang@ucsd.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules endothéliales › Podosomes › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Cellules › Cellules cultivées › Cellules cancéreuses en culture › Lignée cellulaire tumorale › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Peptide hydrolases › Fibroblast activation protein drives tumor...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Processus néoplasiques › Invasion tumorale › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Maladies de la peau et du tissu conjonctif › Maladies de la peau › Maladies du sein › Tumeurs du sein › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Peptide hydrolases › Protéases à sérine › Serine endopeptidases › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Cellules › Cellules du tissu conjonctif › Fibroblastes › Fibroblast activation protein drives tumor...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace extracellulaire › Matrice extracellulaire › Fibroblast activation protein drives tumor...